X-Linked Mental Retardation Gene CUL4B Targets Ubiquitylation of H3K4 Methyltransferase Component WDR5 and Regulates Neuronal Gene Expression

Molecular Cell

Volumn 43, Issue 3, 2011, Pages 381-391

  Nakagawa, Tadashi ^a,b   Xiong, Yue ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE LYSINE METHYLTRANSFERASE; PROTEIN SUBUNIT; PROTEIN WDR5; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN; CONTROLLED STUDY; CUL4B GENE; EPIGENETICS; GENE; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GENETIC STABILITY; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; NEUROSECRETORY CELL; NONHUMAN; PATHOGENESIS; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DEPLETION; RAT; X LINKED MENTAL RETARDATION;

ANIMALS; CULLIN PROTEINS; GENE EXPRESSION REGULATION; GENES, X-LINKED; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; MODELS, MOLECULAR; NERVE GROWTH FACTOR; NEURITES; NEURONS; PC12 CELLS; RATS; UBIQUITINATION;

EID: 79960897683     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.05.033     Document Type: Article

References (66)

1. Abbas T., Shibata E., Park J., Jha S., Karnani N., Dutta A. CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell 2010, 40:9-21.
2. Angers S., Li T., Yi X., MacCoss M.J., Moon R.T., Zheng N. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 2006, 443:590-593.
3. Badura-Stronka M., Jamsheer A., Materna-Kiryluk A., Sowińska A., Kiryluk K., Budny B., Latos-Bieleńska A. A novel nonsense mutation in CUL4B gene in three brothers with X-linked mental retardation syndrome. Clin. Genet. 2010, 77:141-144.
4. Bai S., Ghoshal K., Datta J., Majumder S., Yoon S.O., Jacob S.T. DNA methyltransferase 3b regulates nerve growth factor-induced differentiation of PC12 cells by recruiting histone deacetylase 2. Mol. Cell. Biol. 2005, 25:751-766.
5. Bhoj V.G., Chen Z.J. Ubiquitylation in innate and adaptive immunity. Nature 2009, 458:430-437.
6. Brown S.A., Ripperger J., Kadener S., Fleury-Olela F., Vilbois F., Rosbash M., Schibler U. PERIOD1-associated proteins modulate the negative limb of the mammalian circadian oscillator. Science 2005, 308:693-696.
7. Chen L.-C., Manjeshwar S., Lu Y., Moore D., Ljung B.-M., Kuo W.-L., Dairkee S.H., Wernick M., Collins C., Smith H.S. The human homologue for the Caenorhabditis elegans cul-4 gene is amplified and overexpressed in primary breast cancers. Cancer Res. 1998, 58:3677-3683.
8. Chiurazzi P., Schwartz C.E., Gecz J., Neri G. XLMR genes: update 2007. Eur. J. Hum. Genet. 2008, 16:422-434.
9. Contrepas A., Walker J., Koulakoff A., Franek K.J., Qadri F., Giaume C., Corvol P., Schwartz C.E., Nguyen G. A role of the (pro)renin receptor in neuronal cell differentiation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R250-R257.
10. Cox B.J., Vollmer M., Tamplin O., Lu M., Biechele S., Gertsenstein M., van Campenhout C., Floss T., Kühn R., Wurst W., et al. Phenotypic annotation of the mouse X chromosome. Genome Res. 2010, 20:1154-1164.
11. Davis O.S., Butcher L.M., Docherty S.J., Meaburn E.L., Curtis C.J., Simpson M.A., Schalkwyk L.C., Plomin R. A three-stage genome-wide association study of general cognitive ability: hunting the small effects. Behav. Genet. 2010, 40:759-767.
12. Dou Y., Milne T.A., Tackett A.J., Smith E.R., Fukuda A., Wysocka J., Allis C.D., Chait B.T., Hess J.L., Roeder R.G. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 2005, 121:873-885.
13. Dou Y., Milne T.A., Ruthenburg A.J., Lee S., Lee J.W., Verdine G.L., Allis C.D., Roeder R.G. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol. 2006, 13:713-719.
14. Frescas D., Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 2008, 8:438-449.
15. Furukawa M., Zhang Y., McCarville J., Ohta T., Xiong Y. The CUL1 C-terminal sequence and ROC1 are required for efficient nuclear accumulation, NEDD8 modification, and ubiquitin ligase activity of CUL1. Mol. Cell. Biol. 2000, 20:8185-8197.
16. Furukawa M., He Y.J., Borchers C., Xiong Y. Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat. Cell Biol. 2003, 5:1001-1007.
17. Gambino F., Pavlowsky A., Béglé A., Dupont J.L., Bahi N., Courjaret R., Gardette R., Hadjkacem H., Skala H., Poulain B., et al. IL1-receptor accessory protein-like 1 (IL1RAPL1), a protein involved in cognitive functions, regulates N-type Ca2+-channel and neurite elongation. Proc. Natl. Acad. Sci. USA 2007, 104:9063-9068.
18. Garapaty S., Xu C.F., Trojer P., Mahajan M.A., Neubert T.A., Samuels H.H. Identification and characterization of a novel nuclear protein complex involved in nuclear hormone receptor-mediated gene regulation. J. Biol. Chem. 2009, 284:7542-7552.
19. Greene L.A. Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. J. Cell Biol. 1978, 78:747-755.
20. Hannah J., Zhou P. Regulation of DNA damage response pathways by the cullin-RING ubiquitin ligases. DNA Repair (Amst.) 2009, 8:536-543.
21. He Y.J., McCall C.M., Hu J., Zeng Y., Xiong Y. DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 2006, 20:2949-2954.
22. Higa L.A., Wu M., Ye T., Kobayashi R., Sun H., Zhang H. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 2006, 8:1277-1283.
23. Hu J., McCall C.M., Ohta T., Xiong Y. Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat. Cell Biol. 2004, 6:1003-1009.
24. Hu J., Zacharek S., He Y.J., Lee H., Shumway S., Duronio R.J., Xiong Y. WD40 protein FBW5 promotes ubiquitination of tumor suppressor TSC2 by DDB1-CUL4-ROC1 ligase. Genes Dev. 2008, 22:866-871.
25. Hung M.S., Mao J.H., Xu Z., Yang C.T., Yu J.S., Harvard C., Lin Y.C., Bravo D.T., Jablons D.M., You L. Cul4A is an oncogene in malignant pleural mesothelioma. J. Cell. Mol. Med. 2009, in press. Published online November 19, 2009.
26. Inlow J.K., Restifo L.L. Molecular and comparative genetics of mental retardation. Genetics 2004, 166:835-881.
27. Isidor B., Pichon O., Baron S., David A., Le Caignec C. Deletion of the CUL4B gene in a boy with mental retardation, minor facial anomalies, short stature, hypogonadism, and ataxia. Am. J. Med. Genet. A. 2010, 152A:175-180.
28. Iwase S., Lan F., Bayliss P., de la Torre-Ubieta L., Huarte M., Qi H.H., Whetstine J.R., Bonni A., Roberts T.M., Shi Y. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 2007, 128:1077-1088.
29. Jackson S., Xiong Y. CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci. 2009, 34:562-570.
30. Jin J., Arias E.E., Chen J., Harper J.W., Walter J.C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 2006, 23:709-721.
31. Kaneko-Oshikawa C., Nakagawa T., Yamada M., Yoshikawa H., Matsumoto M., Yada M., Hatakeyama S., Nakayama K., Nakayama K.I. Mammalian E4 is required for cardiac development and maintenance of the nervous system. Mol. Cell. Biol. 2005, 25:10953-10964.
32. Kim K., Choi J., Heo K., Kim H., Levens D., Kohno K., Johnson E.M., Brock H.W., An W. Isolation and characterization of a novel H1.2 complex that acts as a repressor of p53-mediated transcription. J. Biol. Chem. 2008, 283:9113-9126.
33. Kleine-Kohlbrecher D., Christensen J., Vandamme J., Abarrategui I., Bak M., Tommerup N., Shi X., Gozani O., Rappsilber J., Salcini A.E., Helin K. A functional link between the histone demethylase PHF8 and the transcription factor ZNF711 in X-linked mental retardation. Mol. Cell 2010, 38:165-178.
34. Kotake Y., Cao R., Viatour P., Sage J., Zhang Y., Xiong Y. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 2007, 21:49-54.
35. Kotake Y., Zeng Y., Xiong Y. DDB1-CUL4 and MLL1 mediate oncogene-induced p16INK4a activation. Cancer Res. 2009, 69:1809-1814.
36. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
37. Leonard H., Wen X. The epidemiology of mental retardation: challenges and opportunities in the new millennium. Ment. Retard. Dev. Disabil. Res. Rev. 2002, 8:117-134.
38. Liu J., Furukawa M., Matsumoto T., Xiong Y. NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol. Cell 2002, 10:1511-1518.
39. Liu L., Lee S., Zhang J., Peters S.B., Hannah J., Zhang Y., Yin Y., Koff A., Ma L., Zhou P. CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol. Cell 2009, 34:451-460.
40. Michel J.J., Xiong Y. Human CUL-1, but not other cullin family members, selectively interacts with SKP1 to form a complex with SKP2 and cyclin A. Cell Growth Differ. 1998, 9:435-449.
41. Nakayama K.I., Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 2006, 6:369-381.
42. O'Connell B.C., Harper J.W. Ubiquitin proteasome system (UPS): what can chromatin do for you?. Curr. Opin. Cell Biol. 2007, 19:206-214.
43. Oda H., Hübner M.R., Beck D.B., Vermeulen M., Hurwitz J., Spector D.L., Reinberg D. Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 2010, 40:364-376.
44. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
45. Qi H.H., Sarkissian M., Hu G.Q., Wang Z., Bhattacharjee A., Gordon D.B., Gonzales M., Lan F., Ongusaha P.P., Huarte M., et al. Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 2010, 466:503-507.
46. Qiu J., Shi G., Jia Y., Li J., Wu M., Li J., Dong S., Wong J. The X-linked mental retardation gene PHF8 is a histone demethylase involved in neuronal differentiation. Cell Res. 2010, 20:908-918.
47. Ropers H.H. X-linked mental retardation: many genes for a complex disorder. Curr. Opin. Genet. Dev. 2006, 16:260-269.
48. Saita S., Shirane M., Natume T., Iemura S., Nakayama K.I. Promotion of neurite extension by protrudin requires its interaction with vesicle-associated membrane protein-associated protein. J. Biol. Chem. 2009, 284:13766-13777.
49. Sánchez C., Sánchez I., Demmers J.A., Rodriguez P., Strouboulis J., Vidal M. Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol. Cell. Proteomics 2007, 6:820-834.
50. Tahiliani M., Mei P., Fang R., Leonor T., Rutenberg M., Shimizu F., Li J., Rao A., Shi Y. The histone H3K4 demethylase SMCX links REST target genes to X-linked mental retardation. Nature 2007, 447:601-605.
51. Tai H.C., Schuman E.M. Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat. Rev. Neurosci. 2008, 9:826-838.
52. Tarpey P.S., Raymond F.L., O'Meara S., Edkins S., Teague J., Butler A., Dicks E., Stevens C., Tofts C., Avis T., et al. Mutations in CUL4B, which encodes a ubiquitin E3 ligase subunit, cause an X-linked mental retardation syndrome associated with aggressive outbursts, seizures, relative macrocephaly, central obesity, hypogonadism, pes cavus, and tremor. Am. J. Hum. Genet. 2007, 80:345-352.
53. Thompson B.A., Tremblay V., Lin G., Bochar D.A. CHD8 is an ATP-dependent chromatin remodeling factor that regulates beta-catenin target genes. Mol. Cell. Biol. 2008, 28:3894-3904.
54. Trievel R.C., Shilatifard A. WDR5, a complexed protein. Nat. Struct. Mol. Biol. 2009, 16:678-680.
55. Wang Y.L., Faiola F., Xu M., Pan S., Martinez E. Human ATAC Is a GCN5/PCAF-containing acetylase complex with a novel NC2-like histone fold module that interacts with the TATA-binding protein. J. Biol. Chem. 2008, 283:33808-33815.
56. Wei N., Serino G., Deng X.W. The COP9 signalosome: more than a protease. Trends Biochem. Sci. 2008, 33:592-600.
57. Wilkins A., Ping Q., Carpenter C.L. RhoBTB2 is a substrate of the mammalian Cul3 ubiquitin ligase complex. Genes Dev. 2004, 18:856-861.
58. Wysocka J., Swigut T., Milne T.A., Dou Y., Zhang X., Burlingame A.L., Roeder R.G., Brivanlou A.H., Allis C.D. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 2005, 121:859-872.
59. Xiong Y. Targeting p21 degradation locally. Dev. Cell 2010, 19:641-643.
60. Yasui K., Arii S., Zhao C., Imoto I., Ueda M., Nagai H., Emi M., Inazawa J. TFDP1, CUL4A, and CDC16 identified as targets for amplification at 13q34 in hepatocellular carcinomas. Hepatology 2002, 35:1476-1484.
61. Yi J.J., Ehlers M.D. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol. Rev. 2007, 59:14-39.
62. Zheng N., Schulman B.A., Song L., Miller J.J., Jeffrey P.D., Wang P., Chu C., Koepp D.M., Elledge S.J., Pagano M., et al. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 2002, 416:703-709.
63. Zhou P., Howley P.M. Ubiquitination and degradation of the substrate recognition subunits of SCF ubiquitin-protein ligases. Mol. Cell 1998, 2:571-580.
64. Zimmerman E.S., Schulman B.A., Zheng N. Structural assembly of cullin-RING ubiquitin ligase complexes. Curr. Opin. Struct. Biol. 2010, 20:714-721.
65. Zou Y., Liu Q., Chen B., Zhang X., Guo C., Zhou H., Li J., Gao G., Guo Y., Yan C., et al. Mutation in CUL4B, which encodes a member of cullin-RING ubiquitin ligase complex, causes X-linked mental retardation. Am. J. Hum. Genet. 2007, 80:561-566.
66. Zou Y., Mi J., Cui J., Lu D., Zhang X., Guo C., Gao G., Liu Q., Chen B., Shao C., Gong Y. Characterization of nuclear localization signal in the N terminus of CUL4B and its essential role in cyclin E degradation and cell cycle progression. J. Biol. Chem. 2009, 284:33320-33332.